Acceptability of COVID-19 Vaccination among Healthcare Workers in Sudan: A Cross Sectional Survey

Introduction: Following emergency approval of COVID-19 vaccines, several studies have investigated COVID-19 vaccine acceptance and hesitancy especially among healthcare workers (HCWs). Nevertheless, the acceptability of the COVID-19 vaccine by HCWs in Sudan remains unclear. This study aims to investigate the acceptability of the COVID-19 vaccine and it’s determinants among the HCWs. Methods: A web-based cross sectional study design was used to study COVID-19 vaccine hesitancy and its associated determinants. The semi-structured questionnaire was distributed electronically, data collection took place from March-April 2021. Results: A total of 576 HCWs have responded to the survey with mean age of 35 years. The majority were females (53.3%), Medical Doctors (55.4%), and located in the capital state; Khartoum (76.0%). The absolute refusal of COVID-19 vaccine was expressed by 16% of the respondents while 57% were willing to get vaccinated. Males were twice to four times more likely to accept the vaccine. Lower acceptability of COVID-19 vaccine was signicantly associated with the nursing profession (OR= 0.35, 95% CI:0.15-0.82, P<0.00), increased perceived harm from the vaccine (OR= 0.11, 95% CI: 0.05-0.23, P <0.00), lack of condence in the source of vaccine (OR= 0.16, 95% CI:0.08-0.31, P=0.00), organizations and government supervising COVID-19 vaccination process ( OR=0.31, 95% CI:0.17-0.58 P=0.00). Conclusion: This study highlights a moderate level of COVID-19 vaccine acceptability by the HCWs in Sudan. Effective communication of correct, regular, up-to-date evidence on the safety and effectiveness of vaccines is crucial to building trust in vaccines. Special consideration should be in place to address vaccine hesitancy among female HCWs and the nursing profession.


Introduction
The novel coronavirus that was rst emerged in December 2019 and developed into a global pandemic of coronavirus disease 2019 (COVID-19) by March 2020 (1). Since then, the number of COVID-19 cases has been escalating and by 27th of June 2021, the global number of cases exceeded 179 million con rmed cases with 4 million con rmed deaths (2). The rapid transmission of the disease and the high risk to global health have pushed the governments to implement harsh restrictions and regulations to control the pandemic including social distancing and massive use of facemasks. Despite all the preventive measures, the pandemic still developing and claiming more lives worldwide particularly among the rst responders, the Healthcare Workers (HCWs) (3).
First infections of COVID-19 in Sudan were detected among international travelers and returnees who arrived in the country between February and March 2020 (4). Soon later, Sudan has suffered from the widespread of infections and the local dramatic development of the pandemic in lack of adherence among the public community and noncompliance of the individuals to the prevention measures that were promoted by the Ministry of Health (5). respondents, the questionnaire was distributed through professional social media platforms that were exclusive for Sudanese HCWs.

Survey Instrument:
A semi-structured questionnaire was adopted from previous studies (14,19). The questionnaire was selfadministered through a Google form and it has three major sections: (A) Background characteristics include demographic and professional information related to the knowledge and training about COVID-19 and its vaccine. (B) COVID-19 Vaccine acceptance measured with two questions: Would you take the COVID-19 vaccine when it is available (Yes, maybe, No)? and would you advise your family and friends to take the vaccine (Yes, maybe, No)? and (C) Health believes model which was used to explore the determinants for Covid-19 vaccinations acceptability. The model explored the following items: the perceived susceptibility measured by considering oneself at risk to get COVID-19 infection and the need to take the vaccine. Perceived severity was measured as the expected outcome if the subjects contracted COVID-19 infection. Perceived harm was measured by concerns related to the safety and side effects of the vaccine. The perceived bene t was measured as beliefs in the vaccine e cacy and effectiveness.
Cues to action which was measured as whom subjects are intending to protect by taking the vaccine. Perceived barriers were focused on potential lack of con dence in the vaccine producers, government and organizations supervising the vaccination process. Additionally, the open-end broad question: Do you have any comment regarding COVID-19 vaccination in Sudan? was used to qualitatively explore HCWs different perspectives on vaccine acceptability and hesitancy.

Data analysis:
Data from the google sheet was cleaned and entered into IBM® SPSS® Statistics (version 25).
Descriptive analysis: This was performed in form of frequency tables was done for categorical variables.
Means (M) and standard deviations (SD) were estimated for the continuous variables such as age and years of working experience. For the open-end broad question: Do you have any Comments regarding COVID-19 vaccination in Sudan? Answers were translated (if were in Arabic), coded, and common themes were identi ed.
Inferential analysis: Bivariate analysis and multivariable logistic regression analysis was performed to test for determinants of acceptance of COVID-19 vaccination. Only de nitive Yes/No responses were included in this analysis excluding the "maybe" answers. Cross tabulation and Persons Chi-Square test was done to test associations between the outcome variables. Crude Odds Ratio (OR) was used as the estimate of the association. A P value < 0.05 was used as an indicator for the level of signi cance. These associations have been further adjusted using Multivariable logistic regression. Adjusted Odds Ratio (AOR), 95% CI for the AOR, and a signi cant level of P < 0.05 were used. Ethical Considerations: The survey was conducted by the Expanded Programme of Immunization (EPI), Federal Ministry of Health as part of the country's immediate response strategy for the COVID-19 pandemic including the preparation for vaccination throughout the country. Therefore, the need for ethical approval was waived by the National COVID-19 Response Committee. However, informed consent with study explanatory statements was shared with HCWs before their voluntary enrollment in this study. Only HCWs who read and sign this informed consent and provided their responses to the questionnaire were included in this study.
Parameters associated with acceptability of COVID-19 vaccine Bivariate analysis (Table 2) showed that the mean age for those who would accept the vaccine was 36.5 years while the average age of refusers was 34.1 years, P < 0.05. The gender of the participant was found to be strongly associated with the acceptance rate with 85.8% of men accepting the vaccine compared to 70.5% among the female participants. Vaccine acceptance signi cantly increased with years of working experience (Difference in Means = 2.2, P < 0.05), receiving training related to COVID-19 vaccination, and taking care of COVID-19 patients directly or indirectly, p < 0.05. Those who rated their knowledge about the COVID-19 vaccination as excellent were signi cantly the least willing to be vaccinated (59.4%), P < 0.05.  .25, P = 0.00), and the perceived bene t from the vaccine. HCWs acceptance for the vaccine signi cantly reduced with increased perceived harm from the vaccine (OR = 0.11, 95%CI: 0.05-0.23, P = 0.00), lack of con dence in the vaccine producers (OR = 0.16, 95%CI:0.08-0.31, P = 0.00), the organizations and the government supervising COVID-19 vaccination process (OR = 0.31, 95%CI:0.17-0.58, P = 0.00) ( Table 3). 0.00 1 reference =disagree 2 Perceived harm were described as "high" if the answer was "Agree" to all three items constructs, otherwise was described as " low " 3 reference  Among the Health Beliefs determinants, only perceived harm, perceived lack of con dence in vaccine producers, and all cues to take the vaccine continued to be statistically signi cant. Acceptability was signi cantly reduced with lack of con dence in the vaccine producers, OR = 0.19, 95%CI: 0.07-0.47, P = 0.00) ( Table 4). This was even higher than the signi cant negative impact of perceived harms from the vaccine (OR = 0.35, 95%CI: 0.13-0.96, P = 0.04). The main cue to accepting the vaccine by HCWs was to protect their families (OR = 85.09, 95%CI: 27.30-264.70, P = 0.00) ( Table 4). A breakdown of the analysis for each variable can be found in Table 4.

Hcws' Concerns About Covid-19 Vaccination In Sudan
Besides the participants concerns about the safety and the possible side effects of the vaccine, some additional concerns about other aspects were expressed in the comments section of the questionnaire as follows: A 37 years old male doctor. Stated "I think there is a hidden agenda behind COVID-19 vaccine", and a 35 years old female doctor was concerned about the effect of vaccine storing conditions on its safety and e cacy "I am concerned about the storage of the vaccine". Furthermore, two participants were worried about potential corruption related to vaccine distribution, which may lead to unequal distribution of the vaccine. Moreover, many participants emphasized the importance of information dissemination and increasing the awareness of the population to ght false rumors about the vaccine. Additionally, a female doctor suggested that all HCWs be tested for the COVID-19 IgG before vaccination. Lastly, a 39 years old female doctor stated that "For me, to be vaccinated or not is mainly dependent on the type of vaccine available. I do prefer the Oxford vaccine rather than the Pit zer vaccine".

Discussion
The healthcare workers were among the most affected groups by the ongoing COVID-19 pandemic worldwide (20). Since its start in Sudan in March 2020, HCWs were burdened with COVID-19 mortality and morbidity (3,4,21). The current surge of COVID-19 cases leads to severe disruption of collateral health services (5,22). Implementing preventive measures to protect HCWs was a real challenge, which was further complicated by the global shortage of Personal Protective Equipments (PPEs) (23). The rapid development of the COVID-19 vaccine has raised as one of the major strategies to reduce morbidity and mortality due to this pandemic (6,24). Low-and middle-income countries (LMICs) including Sudan were challenged to strategically bene t from the vaccine to stop or at least to slow the current pandemic due to di culties in achieving the optimal coverage among the most at-risk populations, mainly the front-line responders (25). Globally, efforts have been made for equitable access to the vaccine, with a main global understanding that "no one is safe until everyone is safe '. Sudan has joined the COVAX AMC initiative in December 2020 and received 828,000 doses of the AstraZeneca vaccine through the initiative support (18), which is only enough to vaccinate less than 1% of the country population. Considering this limitation of vaccine supply, the national committee for COVID-19 deployment and vaccination plan has prioritized the HCWs and most vulnerable groups (elders with co-morbidities) for the rst phase of the vaccination to maintain the health service, reducing deaths and disease severity among the vulnerable group. Despite these efforts to make vaccines available for this key target group, vaccine acceptance by the HCWs would signi cantly affect its uptake. COVID-19 vaccination hesitancy has been of increasing concern in many countries (13,14). In this survey, we measured the extent of acceptability of COVID-19 vaccination among HCWs in Sudan. We also identi ed key factors that could affect HCW's decision to take the vaccine. This is expected to support the development of evidence-based COVID-19 vaccination advocacy to ensure optimal acceptance of COVID-19 vaccine among HCWs in Sudan The majority of respondents were young with average age of 35.3 years, direct or indirect caretakers of COVID-19's patients and 20% of them had a history of COVID-19 infection. Females represented more than half of the respondents and this matches the gender representation of the health workforce in Sudan. Sixteen percent expressed absolute refusal, which is double the percentage reported by HCWs in the US (14,26). In contrast, 57% of the Sudanese HCWs will take the vaccine as soon as it is available. This relatively high acceptance rate is comparable to what has been reported by UNICEF in Ghana (27), and double the acceptance rate reported among Congolese HCWs (13). The latter has the lowest reported HCWs' vaccine acceptance globally (11). Nurses' likelihood to accept the vaccine was almost zero. They were the category of HCWs with the least acceptance rate for the vaccine.
To increase COVID-19 vaccine acceptance, positive reinforcement of public perceptions through effective communications of the correct and up-to-date evidence on the safety and effectiveness of the vaccines is crucial. Exposure to misinformation about the vaccine can lower COVID-19 acceptance by up to 6% (28). In this study, HCWs' acceptance was inversely correlated with their self-rated Knowledge about COVID-19 vaccination. It was clear that HCWs have built negative perceptions regarding the COVID-19 vaccine. This was translated into concerns regarding the process of development and safety of the vaccine, as more than half of the participants were worried about the vaccine's side effects. More than a quarter were worried about how rapidly the vaccine was developed. Perceived mistrust towards vaccine manufacturers and increased perceived harms from the vaccine reduced the vaccine acceptance by almost 80% and 65%, respectively. However, this is a global challenge given the fact that the vaccine for COVID-19 was developed within the shortest time in human history. This calls for putting extra effort to build public trust for the vaccine. The advocacy phase should focus on providing up-to-date information about vaccine safety. Implementation-wise, well-functioning adverse events and rumors tracking systems are vital.
Female HCWs were twice less likely to take the vaccine compared to their male colleagues. This might be explained by the gender disparities in perceived vaccine safety. Adverse events from COVID-19 vaccines have been unduly reported among Women compared to men, and it has been excessively covered in the news (29)(30)(31). The latter could have disproportionately built a negative perception of vaccine safety among females compared to males. It is crucial to take gender differences into account when addressing COVID-19 vaccine acceptance, as women represent the majority of the healthcare workforce in the country (26). This high hesitancy puts them at a higher risk of COVID-19 morbidity and mortality.
In conclusion, the acceptability of COVID-19 vaccination among HCWs in Sudan was average and comparable to others globally. Vaccine advocacy among HCWs needs to be aligned with the identi ed determinants. Acceptability was negatively determined by the female gender, the nursing profession, and knowledge about COVID-19 vaccination. Also, acceptability was signi cantly reduced by the increased perceived harm from the vaccine and the increased mistrust for the vaccine manufacture.
Strengths and Limitations: Little is known about the acceptability of COVID-19 vaccination among HCWs in LIMICs. The major strength of this study is that this survey is the rst post vaccine availability survey to address determinants of COVID-19 vaccination acceptability among HCWs in Sudan. A potential limitation of this study is that the questionnaire was distributed in an online format which could introduce selection bias by excluding HCWs who do not have access to the internet.

Declarations
Con ict of interest: Authors have no con ict of interest to declare Funding: This research did not receive any speci c grant from funding agencies in the public, commercial, or not-for-pro t sector.